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ORIGINAL RESEARCH published: 02 April 2019 doi: 10.3389/fmars.2019.00114

The Contribution of Fine Sieve Fractions (63–150 µm) to Foraminiferal Abundance and Diversity in an Area of the Eastern Pacific Ocean Licensed for Polymetallic Nodule Exploration

Andrew J. Gooday* and Aurélie Goineau

National Centre, University of Southampton, Waterfront Campus, Southampton, United Kingdom

The sieve mesh sizes used in benthic foraminiferal studies exert a strong influence on faunal densities and composition. We examined the consequences of including Edited by: finer (63–150 µm) size classes in a study of Rose Bengal stained (‘live’) and dead Randi D. Rotjan, in 5 Megacorer samples (0–1 cm layer) from abyssal sites in the eastern Boston University, United States Clarion-Clipperton Zone (CCZ; equatorial Pacific), a region with commercially significant Reviewed by: Ellen Pape, deposits of polymetallic nodules. More than 60% of intact specimens originated from Ghent University, Belgium the finer (<150 µm) fractions, with over half being picked from 63 to 125 µm residues. Akkur Vasudevan Raman, Test fragments, mainly agglutinated tubes, were also abundant but were more evenly Andhra University, India distributed between coarser and finer residues. The two fractions yielded the same *Correspondence: Andrew J. Gooday main groups (a mixture of formal taxa and informal groupings) and were dominated [email protected] by single-chambered forms (‘monothalamids’), the majority undescribed. Some were disproportionately abundant in finer fractions: rotaliids in the stained (‘live’), textulariids in Specialty section: This article was submitted to the dead, and trochamminids, Lagenammina spp., Nodellum-like forms, saccamminids Deep-Sea Environments and Ecology, and spheres in both assemblages. However, the most striking difference was the much a section of the journal Frontiers in Marine Science greater abundance of tiny, largely undescribed spherical agglutinated morphotypes in Received: 05 October 2018 the <150-µm fractions. Our 5 samples yielded 462 morphospecies, of which 313 Accepted: 25 February 2019 occurred in <150-µm fraction and 170 were confined to this fraction. Twelve of the Published: 02 April 2019 31 top-ranked species in the stained assemblage were more or less limited (>90%) to Citation: the finer fractions; the corresponding number for the stained + dead assemblage was Gooday AJ and Goineau A (2019) The Contribution of Fine Sieve 12 out of 35. Of the 46 most abundant species in the stained + dead assemblage, Fractions (63–150 µm) 35 were monothalamids (mainly spheres, Lagenammina spp., Nodellum-like forms, and to Foraminiferal Abundance and Diversity in an Area of the Eastern saccamminids), the remainder being rotaliids (3), hormosinids (3), trochamminids (3) and Pacific Ocean Licensed textulariids (2). By far the most abundant species overall, a tiny agglutinated sphere, for Polymetallic Nodule Exploration. was almost entirely confined to the finer fractions. Although small foraminifera that pass Front. Mar. Sci. 6:114. doi: 10.3389/fmars.2019.00114 through a 150-µm screen are time-consuming to analyze, they constitute an important

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Gooday and Goineau Foraminifera in Fine Sieve Fractions

part of abyssal Pacific assemblages and may include opportunistic species that respond to episodic food pulses as well as pioneer recolonizers of defaunated substrates. It is therefore important to consider them in studies of possible mining impacts on abyssal benthic communities.

Keywords: polymetallic nodules, Clarion-Clipperton Zone, baseline survey, abyssal benthic foraminifera, sieve mesh size, biodiversity, recolonization

INTRODUCTION areas, also in the eastern CCZ, licensed by the International Seabed Authority for seabed exploration to the UK Seabed The use of different sized meshes to sieve sediment samples is an Resources Ltd. (UK-1 area), and Ocean Mineral Singapore Pte important issue in meiofaunal research, the mesh acting as a filter Ltd. (OMS area). The UK-1 area was sampled in 2013 and that strongly influences important assemblage metrics, notably both areas were sampled in 2015 during ABYSSLINE research faunal densities, biomass, diversity and taxonomic composition cruises. Previous studies on meiofaunal foraminifera within of taxa such as nematodes (Leduc et al., 2010). A mesh size the framework of this project have described novel species of 32 µm is now the widely accepted lower limit for the that use radiolarian shells as microhabitats (Goineau and metazoan meiofauna. In the case of foraminifera, however, Gooday, 2015) and foraminiferal composition and diversity different studies have used a variety of different sized meshes in >150 µm size fractions (Goineau and Gooday, 2017). Here, (Sen Gupta et al., 1987). The most common are 150, 125, and we extend this earlier research by describing assemblages of 63 µm, although larger (250 or 300 µm; e.g., Bernstein et al., stained and dead benthic foraminifera retained on 63 and 1978; Lutze and Coulbourne, 1984; Gooday et al., 2001) or smaller 125 µm mesh sieves and comparing them with assemblages in (45 or 32 µm; e.g., Gooday, 1986; Pawlowski and Lapierre, residues >150 µm. We address two main questions. (1) How 1988; Pawlowski, 1991; Gooday et al., 1995; Nozawa et al., much information on foraminiferal abundance and diversity 2006; Szarek et al., 2007) sizes have been adopted occasionally. is added by analyzing these finer fractions? (2) What are the The need to analyze finer sieve fractions (63–125 µm or 63– differences in foraminiferal assemblage composition between the 150 µm) becomes more pressing in deep-sea settings, where larger and smaller size fractions? benthic organisms are generally small in size compared to shallower waters (Thiel, 1975, 1983; Shirayama and Horikoshi, 1989). Although this involves a larger investment of time MATERIALS AND METHODS compared to the analysis of larger-sized fractions, Schröder et al. (1987) argue that the extra effort is worthwhile because valuable General information about the ABYSSLINE project is given by faunal information, including a large proportion of specimens Glover et al. (2015). For environmental information about the belonging to environmentally important ‘indicator’ species, is study area see Amon et al. (2016) and Goineau and Gooday lost by ignoring sieve residues <150 µm. For example, at (2017). Pape et al. (2017) provide further environmental data bathyal depths in the North Atlantic, small-sized species include (sediment granulometry, porosity and sorting, total organic several that respond opportunistically to seasonally pulsed food carbon and total nitrogen content) for the GSR license area, inputs (Gooday and Hughes, 2002; Duchemin et al., 2007; located to the west of the UK-1 and OMS areas and in somewhat Phipps et al., 2012). deeper water (∼4500 m). In general terms, our shipboard and Relatively few studies based on fine sieve fractions have been laboratory methods followed those described by Goineau and undertaken in the Pacific Ocean. Snider et al. (1984) analyzed Gooday (2017). We use the term ‘stained’ to refer to specimens the 45–150 and 150–300 µm fractions for meiofaunal organisms, that were inferred to be alive when stained. mainly foraminifera, many of them single-chambered forms (monothalamids). More recently, Nozawa et al. (2006) used Sampling a 32 µm mesh in a study of foraminifera, again dominated Samples were collected during two ABYSSLINE cruises at 5 sites by monothalamids, from the ‘Kaplan East’ site in the eastern (Supplementary Table S1) in three 30 × 30 km study areas Clarion-Clipperton Zone (CCZ, abyssal equatorial Pacific), (‘strata’) located within the UK-1 and OMS exploration contract a region where large tracts of seafloor are covered with areas (Figure 1). Two were obtained in Stratum A of the UK-1 commercially significant deposits of polymetallic nodules. license area, centered around 13◦490 N, 116◦360 W, during the Radziejewska et al. (2006) presented some preliminary first cruise (AB01, R/V Melville, cruise MV1313, 3–27 October observations of monothalamids and other foraminifera based 2013), two in UK-1 Stratum B, centered around 12◦ 28.90 N, 116◦ on the >32-µm fractions of samples from the same general 36.30 W, and one in the OMS Stratum, centered around 12◦ 8.20 area. Ohkawara et al. (2009) described a tiny new spherical N, 117◦ 17.70 W during the second cruise (AB02: R/V Thomas monothalamid that was abundant in samples from the Kaplan G Thompson cruise TN319; 12 February to 25 March, 2015). Central site in the deeper and more central part of the CCZ. In each case the samples were recovered using a hydraulically The present contribution is part of the AYSSLINE (ABYSSal dampened Megacorer (BCMEGA OSIL Bowers & Connelly type), baseLINE) project, a baseline survey of foraminifera in two equipped with 12 polycarbonate coring tubes. As soon as possible

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FIGURE 1 | (Left) Location of the Ocean Mineral Singapore (OMS) and UK-1 exploration contract areas in the eastern Clarion-Clipperton Zone, equatorial Pacific. (Right) Location of UK-1 Strata A and B and the OMS stratum within the two contract areas.

after collection, the cores were sliced, using a metal plate, into observations of test morphology and wall structure, and assigned 0.5-cm thick layers to 2 cm depth and 1-cm thick layers from to genera or species where possible. Those that could not be 2 to 10 cm depth and each layer preserved separately in a placed in known taxa were given a descriptive working name. 500 ml plastic bottle with 10% formalin buffered with borax. Any Some of the methodological challenges involved in analyzing nodules present in the core were carefully removed in order to benthic foraminifera in sediment residues from the abyssal CCZ facilitate slicing and sediment adhering to them washed into the are outlined in the Supplementary Material. appropriate sample bottle. Statistical Methods Laboratory Processes T-tests to compare the relative abundances of major groups in The 0–0.5 and 0.5–1.0 cm sediment layers were used for this the >150 and <150 µm fractions were computed using Excel. study. In the laboratory, the volume of each slice was measured Based on complete specimens only (stained and stained plus by settling the sediment in a graduated cylinder for 2 days dead combined), we used the open source software EstimateS (after which the volume stabilized) followed by splitting into 8 (Version 9) (Colwell et al., 2012) to calculate the Fisher alpha (α) parts using a wet splitter (Jensen, 1982). One split was selected and Shannon (H’, using natural logarithm) diversity indices, and for analysis and its volume measured in the same way. It was rarefied species richness values [E(S100)] – the expected number then sieved on a series of meshes (300, 150, 125, 63 µm) and of species represented by 100 individuals) using the open source each residue stained overnight on the sieve in Rose Bengal software EstimateS (Version 9) (Colwell et al., 2012). solution (1 g in 1 l of tapwater). The stained residues were transferred in water to a Petrie dish and examined under a stereo-microscope. All foraminifera (stained and unstained) and RESULTS metazoan meiofaunal animals were removed using a glass pipette. In most cases they were stored on cavity slides in a small Abundance volume of glycerol, the cavities being left uncovered in order We picked a total of 2341 complete stained (‘live’) foraminiferal to allow easy access to the specimens. Some delicate organic- tests, 1093 complete dead tests, and 1381 fragments (stained walled foraminifera that shrank in glycerol were placed in 1.25 ml and dead combined) from the >300, 150–300, 125–150, and Nalgene R cryovials, while calcareous foraminifera, which were 63–125 µm fractions combined of the five 1/8th sample splits. rare, were placed on dry slides in order to avoid dissolution Individual splits yielded 269–777 (=274–791.10 cm−2) stained in the glycerol. Foraminifera with stained cytoplasm and (if tests, 125–329 (=127–335.10 cm−2) dead tests and 115–497 present) fresh stercomata were considered to have been alive (=117–506.10 cm−2) test fragments. when sampled (see Supplementary Material for discussion of A majority (62.2%) of complete stained foraminiferal tests criteria for distinguishing stained from dead tests). originated from the two finer sieve fractions (<150 µm; All foraminiferal specimens were examined under an i.e., 63–125 and 125–150 µm combined), with more Olympus BH-2 compound microscope and photographed using than half (52.7% overall) being found in the 63–125 µm an SLR digital camera (Canon EOS 350D) attached to the fraction alone (Table 1). The dead assemblage showed a microscope. Calcareous and delicate organic-walled foraminifera similar proportion; 64.8% overall in the two finer fractions were placed in a cavity slide with water for this purpose, but the with 53.7% in the 63–125 µm fraction. Fragmented tests majority of specimens were photographed in glycerol. Specimens (live + dead combined, mainly tube fragments) were more were grouped into working morphospecies based mainly on evenly distributed between the two fractions, with 47.5%

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TABLE 1 | Numbers and percentages of complete foraminiferal tests (stained + dead) in the 5 sample splits of which the >150 µm and 63–150 µm fractions were analyzed.

N range %range Mean N Mean%

Stained 300 µm 8–56 2.48–7.99 29.8 6.15 37.8% >150 µm 150–300 µm 43–284 13.3–35.3 153 31.6 125–150 µm 26–72 4.97–13.6 46.0 9.49 62.2% <150 µm 63–125 µm 137–330 44.5–70.6 121 52.7 Dead 300 µm 7–17 3.35–8.08 11.6 5.73 35.2% >150 µm 150–300 µm 39–71 14.5–46.2 55.8 29.5 125–150 µm 13–46 7.92–15.2 22.6 11.1 64.8% <150 µm 63–125 µm 42–190 35.3–70.6 121 53.7

originating from the >150 µm and 52.5% from the <150 µm significantly more abundant in the finer fractions, however, are fraction (Table 2). the saccamminids and spheres (Tables 3, 4). The difference is particularly striking in the case of the stained spheres, which, on Main Groups average, are some 5 times more abundant in the 63–150 µm than Species were divided into a series of main categories, in the >150 µm fraction. This difference is highly significant a mixture of formal taxa (e.g., rotaliids, hormosinids, (p < 0.001) for stained specimens (Table 3) and significant trochamminids) and informal morphology-based groupings (p < 0.05) for the dead specimens (Table 4). These tiny spheres (e.g., spheres, tubes, and ‘other monothalamids’). The form a substantial proportion of the stained assemblage. latter encompasses monothalamids that are difficult to They are largely undescribed and in most cases regarded catorgorise morphologically; some examples are illustrated as indeterminate since it was not possible to consistently in Supplementary Figures S1A–C,E–G, S2A,B. The same distinguish morphologically distinct types amongst them. Some main taxa and morphological groupings are represented in examples of the more common forms are shown in Figure 4 and both the >150 µm and <150 µm fractions (Tables 3, 4). Supplementary Figure S8. Among groups represented by complete tests (stained and Test fragments (stained and dead combined) are dominated dead), most tend to be more abundant in absolute terms by tubes and spindle-shaped morphotypes (grouped together), in the finer fractions. This difference is particularly clear in with lesser contributions from komokiaceans (Baculellidae and the case of rotaliids and trochamminids (Figures 2A,D–H Komokiidae) (Figure 3). However, the only clear differences and Supplementary Figures S3C–E, S4A–D), Lagenammina between fractions are the greater average absolute and relative spp. (Supplementary Figures S5A–F), Nodellum-like forms abundance of baculellid fragments in the coarser fractions (Supplementary Figure S6), saccamminids (Supplementary and, to a lesser extent, of komokiids in the finer fractions Figure S7), spheres (Figure 4; Supplementary Figure S8), (Supplementary Table S2). The differences were not significant and organic-walled forms (Supplementary Figures S9A–E) (p > 0.05), however. In the case of the komokiids, it reflected in the live assemblage, and textualariids (Figures 2B,C and the large number of small fragments of a Reticulum species Supplementary Figures S4E,F), trochamminids, Lagenammina (Figure 3K) in the 63–125 and 125–150 µm fractions of spp., Nodellum-like forms, saccamminids, and spheres in the the MC13 sample. dead assemblage. On the other hand, complete tubes and Table 5 presents data for the calcareous and agglutinated taxa spindles, chains, ‘other monothalamids’ and Komokiacea that have more robust tests and therefore the potential to survive (‘komoki’; families Baculellidae and Komokiidae, putative in the fossil record. We include here all of the multichambered monothalamids; Figure 3K and Supplementary Figure S1D) foraminifera ( and Tubulothalamea) (Figure 2 are more abundant in the coarser fractions, particularly in and Supplementary Figures S3A–E, S4), together with species the case of stained specimens. The only groups that are of Lagenammina (Supplementary Figures S5A–F), which,

TABLE 2 | Numbers and percentages of fragmentary foraminiferal tests (stained + dead) in the 5 sample splits of which the >150 µm and 63–150 µm fractions were analyzed.

N range %range Mean N Mean%

300 µm 15–46 6.38–34.3 34.6 13.0 150–300 µm 20–308 14.9–52.7 160 34.5 47.5% >150 µm 125–150 µm 27–95 8.87–20.1 53.6 15.2 63–125 µm 41–246 24.5–62.1 140 37.3 52.5% <150 µm Total per 10 cm2 17–84

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TABLE 3 | Mean and percentage abundances (±standard deviations) of major groups based on complete stained specimens in the two size fractions and both fractions combined of 5 samples.

All fractions >150 µm 63–150 µm

N%N%N%

Foraminiferal group Rotaliids 12.8 ± 8.47 3.01 ± 2.61 3.80 ± 2.86 3.92 ± 6.83 9.20 ± 5.81 3.12 ± 1.94 Miliolids 1.60 ± 1.34 0.35 ± 0.35 0.40 ± 0.55 0.15 ± 0.23 1.40 ± 1.14 0.44 ± 0.39 Lagenids 0.60 ± 0.89 0.15 ± 0.25 0 0 0.60 ± 0.89 0.20 ± 0.30 Ammodiscids 0.20 ± 0.45 0.04 ± 0.08 0.20 ± 0.45 0.10 ± 0.25 0.20 ± 0.45 0.06 ± 0.13 Textulariids 3.20 ± 1.00 0.65 ± 0.18 1.20 ± 0.45 1.00 ± 0.80 2.40 ± 1.67 0.79 ± 0.45 Trochamminids 5.00 ± 4.36 1.04 ± 1.04 0.40 ± 0.55 0.19 ± 0.28 4.40 ± 4.28 1.32 ± 1.34 Hormosinids 14.8 ± 6.38 3.04 ± 1.16 6.20 ± 5.45 3.28 ± 2.23 6.60 ± 5.37 2.65 ± 1.90 Nodellum-like 14.4 ± 12.1 2.74 ± 2.01 2.4 ± 2.07 1.21 ± 1.17 11.6 ± 10.0 3.64 ± 2.70 Lagenammina 21.0 ± 8.94 4.44 ± 2.19 2.40 ± 1.67 2.56 ± 3.77 18.6 ± 8.17 5.80 ± 1.90 Flasks 16.4 ± 12.7 3.41 ± 2.64 8.40 ± 5.55 5.03 ± 5.10 8.00 ± 9.30 2.32 ± 2.65 Chambers 2 tubes 5.60 ± 3.21 1.15 ± 0.57 1.60 ± 1.82 1.04 ± 1.60 4.00 ± 2.83 1.19 ± 0.67 Saccamminids 17.6 ± 6.58 4.05 ± 1.96 2.20 ± 2.59 0.90 ± 1.18 15.4 ± 8.02 5.39 ± 2.77 Spheres 171 ± 36.8 37.6 ± 8.11 27.8 ± 18.3 14.94 ± 5.86 143 ± 22.1 49.4 ± 13.3 Organic-walled 14.0 ± 7.87 2.88 ± 1.31 3.80 ± 3.90 1.58 ± 0.92 10.2 ± 5.63 3.56 ± 2.13 Hyperammina 0.60 ± 1.34 0.08 ± 0.19 0.20 ± 0.45 0.06 0.40 ± 0.89 0.102 ± 0.22 Tubes/spindles 56.2 ± 38.2 11.1 ± 4.43 38.4 ± 22.4 21.4 ± 5.85 20.2 ± 17.3 6.12 ± 3.82 Other monothalamids 59.8 ± 65.1 10.5 ± 8.40 36.2 ± 38.0 18.2 ± 8.48 23.6 ± 27.4 6.47 ± 6.76 Chains 4.00 ± 3.87 0.69 ± 0.64 2.80 ± 3.83 1.18 ± 2.00 1.20 ± 1.30 0.34 ± 0.34 Komoki-like 14.4 ± 11.5 2.54 ± 1.59 6.25 ± 5.54 3.12 ± 2.51 8.40 ± 8.53 2.37 ± 1.98 Komoki: baculellids 10.4 ± 8.41 1.91 ± 1.05 9.60 ± 8.02 4.52 ± 1.89 0.80 ± 0.83 0.24 ± 0.25 Komoki: komokiids 4.60 ± 1.81 0.97 ± 0.24 4.40 ± 1.95 2.96 ± 1.71 0.20 ± 0.45 0.07 ± 0.15 Radiolarian Inhabitants 22.4 ± 12.4 5.44 ± 2.80 17.6 ± 14.0 10.9 ± 7.10 5.00 ± 6.40 1.69 ± 2.17 Total numbers 2386 929 1457 Gromiids (n = 21) 4.80 ± 4.44 1.08 ± 1.22 0.40 ± 0.89 0.125 4.40 ± 4.16 1.41 ± 1.38

Values that are significantly different between the two fractions are underlined (p < 0.05) or bold and underlined (p < 0.001).

although monothalamous, have more or less rigid test walls spheres, Lagenammina species, and ‘other monothalamids’ make and are known as fossils. Hormosinids (23.2% of stained and up the majority. Most of the multichambered species are 25.1% of dead specimens) and Lagenammina species (40.8% of textulariids, including several Reophax species. By far the most stained and 25.0% of dead specimens) are abundant constituents abundant species, both overall and in particular categories, is of the both stained and dead assemblages when the coarser a small agglutinated sphere (Psammosphaerid sp. 20) that is and finer fractions are combined, and are joined in the dead almost entirely confined (99.4%) to the finer residues. Seven assemblage by the textulariids (21.5%). Rotaliids are relatively other species (Spiroplectammina subcylindrica, ‘lobed spheres,’ more common in the stained (19.6%) than in the dead (8.38%) Lagenammina yellowish with long neck, Lagenammina sp. 9, assemblage. The overall composition of the >150 µm and Saccamminid sp. A, Saccamminid sp. 5) are found exclusively <150 µm assemblages is similar. However, hormosinids are in the <150 µm fractions (stained + dead assemblage). The relatively less abundant in the finer fractions (stained 19.1% 30 most common species (stained + dead) in the <150- vs. 33.7%; dead 23.2% vs. 30.2%), a pattern reversed in the µm fraction include 23 that are also in the top 32 for the case of Lagenammina spp. (stained 42.7% vs. 36.0%; dead combined residues (>150 + <150 µm). In the case of the 30.2% vs. 11.3%). stained-only assemblage in the <150-µm fraction, the top 30 species include 22 that are also among the top-ranked species Common Species in the two residues combined; these include all of the 17 most Supplementary Tables S3–S6 detail the 30 or so most abundant species. abundant species in the stained + dead and stained only assemblages; in each case, data for all fractions combined, Diversity and the <150 µm fraction only, are shown separately. All 44 The five samples combined yielded a total of 462 provisional species listed in these tables are illustrated in Figures 2–4 and morphospecies of testate protists (stained and dead, complete the Supplementary Figures and brief descriptions are given and fragmentary tests) that were regarded as foraminifera. the taxonomic notes included in the Supplementary Material. Of these, 54 were represented only by fragmented specimens, More than three-quarters (34) are monothalamids, among which 279 occurred in the >150 µm fraction, 313 occurred in

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TABLE 4 | Mean and percentage abundances (± standard deviations) of major groups based on complete dead specimens in the two size fractions and both fractions combined of 5 samples.

All fractions >150 µm 63–150 µm

N%N%N%

Foraminiferal group Rotaliids 12.6 ± 19.3 4.83 ± 6.34 5.80 ± 8.58 7.38 ± 10.0 6.80 ± 10.8 3.62 ± 4.58 Miliolids 0.60 ± 0.55 0.28 ± 0.28 0.50 ± 0.55 0.80 ± 0.74 0 0 Lagenids 0.80 ± 1.30 0.31 ± 0.48 0.20 ± 0.45 0.26 ± 0.58 1.00 ± 1.41 0.69 ± 0.98 Ammodiscids 5.80 ± 4.09 2.64 ± 1.47 2.60 ± 2.70 4.03 ± 4.57 4.20 ± 4.44 2.98 ± 2.27 Textulariids 24.6 ± 15.9 11.2 ± 5.95 8.00 ± 2.83 11.8 ± 5.11 17.0 ± 14.4 12.03 ± 8.37 Trochamminids 13.8 ± 11.5 6.22 ± 3.94 4.20 ± 3.56 6.01 ± 5.00 9.60 ± 8.73 6.64 ± 4.01 Hormosinids 30.2 ± 18.3 13.2 ± 4.94 9.80 ± 4.44 14.7 ± 8.32 20.4 ± 15.0 12.6 ± 3.79 Nodellum-like 12.0 ± 7.84 5.87 ± 3.46 0.60 ± 0.89 0.82 ± 1.19 11.4 ± 7.60 8.88 ± 4.58 Lagenammina 29.6 ± 17.8 12.7 ± 3.68 4.80 ± 3.56 6.69 ± 4.42 24.8 ± 12.0 15.1 ± 4.92 Flasks 6.80 ± 3.83 3.52 ± 2.16 2.60 ± 2.07 3.70 ± 2.96 3.60 ± 2.69 2.64 ± 2.72 Chambers 2 tubes 7.00 ± 2.82 3.51 ± 1.48 2.80 ± 2.77 4.16 ± 4.25 4.20 ± 2.81 2.58 ± 1.16 Saccamminids 8.25 ± 3.77 3.85 ± 0.85 1.60 ± 1.67 2.40 ± 2.54 6.80 ± 3.03 4.96 ± 1.43 Spheres 28.8 ± 13.7 13.7 ± 3.57 5.60 ± 2.97 7.76 ± 3.58 23.2 ± 14.3 16.78 ± 7.87 Organic-walled 0.40 ± 0.55 0.16 ± 0.16 0 0 0.40 ± 0.55 0.22 ± 0.32 Hyperammina 1.20 ± 0.84 0.57 ± 0.38 0.60 ± 0.89 0.98 ± 1.48 0.60 ± 0.89 0.36 ± 0.58 Tubes/spindles 11.0 ± 4.85 5.59 ± 2.27 5.40 ± 2.07 7.96 ± 3.22 6.60 ± 5.94 4.85 ± 3.89 Other monothalamids 10.0 ± 2.55 4.91 ± 1.44 6.00 ± 3.39 8.84 ± 5.20 4.00 ± 2.92 2.52 ± 0.95 Chains 1.80 ± 3.49 1.00 ± 2.28 0.80 ± 1.79 1.04 ± 2.32 1.00 ± 1.73 0.92 ± 1.82 Komoki-like 1.80 ± 2.39 0.93 ± 1.64 1.40 ± 2.61 1.80 ± 3.39 0.40 ± 0.55 0.23 ± 0.32 Komoki: baculellids 3.20 ± 3.11 1.55 ± 1.93 2.80 ± 2.68 3.72 ± 3.56 0.40 ± 0.55 0.34 ± 0.49 Komoki: komokiids 2.20 ± 1.79 1.07 ± 0.76 2.00 ± 1.87 2.64 ± 2.20 0.20 ± 0.45 0.13 ± 0.30 Radiolarian inhabitants 2.20 ± 1.79 1.07 ± 0.71 2.20 ± 1.79 3.05 ± 2.47 0 0 Total numbers 1140 413 727 Gromiids 0 0 0 0 0 0

Values that are significantly different are underlined (p < 0.05).

the <150-µm fractions and 170 were confined to these fine an inconsistent influence on R1D values when the two fractions (Table 6). The most diverse groups were the tubes fractions are combined. with 77 species, 20 of them confined to fractions <150 µm, and the spheres, with 61 species, 25 confined to the fine fractions. Among multichambered groups, textulariids (32 Gromiids, Unknown Testate Structures, species, 18 only in <150 µm fractions) and hormosinids and Metazoan Meiofauna (30 species, 6 only in <150 µm fractions) were the most The <150-µm residues yielded 21 specimens with transparent specious. If the >150 µm dataset is expanded to include organic tests that were regarded as gromiids based on the six additional sample splits for which the fine fractions were presence of an oral capsule (Hedley, 1960; Rothe et al., 2010). not analyzed (Goineau and Gooday, unpublished), then the Most had more or less elongate, droplet-like tests that tapered number of morphospecies found only in the >63 µm fraction is toward the oral capsule (Supplementary Figures S9G,I), but halved from 170 to 84. a few were sausage-shaped (Supplementary Figure S9F) or Detailed diversity metrics based on complete individuals spherical (Supplementary Figure S9H). They are tentatively are summarized in Table 7 (stained plus dead specimens assigned to 8 morphospecies, all confined to the fine fractions, combined) and Table 8 (stained specimens only). Species although variability in test morphology made it difficult to 0 numbers and diversity indices [H , Fisher α, E(S100)] are discriminate between some of these forms. generally higher in samples that include the 63–125-µm The fine fractions (mainly the 63–125 µm fraction) of some plus 125–150-µm fractions compared to those based on samples also yielded a variety of more or less spherical, organic- only the 150–300-µm plus >300 µm fractions. Except for walled structures that gave rise to relatively short blind-ending sample MC21, where stained specimens were 3.5 times more processes (Figure 5). They were concentrated in the MC11 and abundant in the finer than the coarser residues, Rank 1 MC13 samples and included three main types. Type A varies Dominance (R1D) is higher in the case of the <150-µm in shape from spherical to oval or somewhat irregular and assemblages. However, inclusion of the finer fractions has is characterized by a variable number (2–10) of short tubular

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FIGURE 2 | Multichambered foraminifera. (A) Epistominella exigua Brady; ‘live’ specimen with green cytoplasm, picked from >150 µm residue at sea. (B) Ammobaculites filiformis Earland; MC09, 0–0.5 cm, 63–125 µm fraction. (C) Spiroplectammina subcylindrica Earland; MC21 G 0–0.5 cm, 63–125 µm. (D) Trochamminacean sp. 1; MC21, 0.5–1.0 cm, 63–125 µm fraction. (E,F) Trochamminacean sp. 2; MC21, 0.5–1.0 cm, 63–125 µm fraction. (G,H) Adercotryma sp.; MC21, 0.5–1.0 cm, 63–125 µm fraction. (G) Rounded specimen. (H) More elongate specimen. (I) Reophax scorpiurus Montfort, MC11, 0.5–1.0 cm, 150–300 µm fraction. (J) Reophax sp. 1, MC05, 0–0.5 cm, >300 µm fraction. Scale bars = 50 µm (A–H), 250 µm (I), 500 µm (J).

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FIGURE 3 | (A–F) Undescribed tubular foraminifera (fragments unless stated otherwise). (A) Stained; MC21, 0.5–1.0 cm, 63–125 µm fraction. (B) Stained with stercomata; MC13, 0–0.5 cm, 125–150 µm fraction. (C) Stained; MC11, 0–0.5 cm, 63–125 µm fraction. (D) Dead; MC13, 0–0.5 cm, 125–150 µm fraction. (E) Stained; MC09, 0–0.5 cm, 63–125 µm fraction. (F) Dead; MC21, 0.5–1.0 cm, 63–125 µm fraction. (G) Stained, complete test; MC05, 0.5–1.0 cm, 63–125 µm fraction. (H) Dead tubular fragment with stercomata; MC11, 0–0.5 cm, 63–125 µm fraction. (I) Complete tubular specimen; MC11, G, 0–0.5 cm, 63–125 µm fraction. (J) Marsipella sp.; MC11, 0–0.5 cm, 63–125 µm fraction. (K) Stained fragment of Reticulum (komokiacean); MC13, 0–0.5 cm, 125–150 µm fraction. Scale bars = 100 µm.

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FIGURE 4 | Undescribed spherical foraminifera from 63 to 125 µm fractions. (A,B) Psammosphaerid sp. 20, the most abundant morphospecies species in the stained assemblage; MC13, 0.5–1.0 cm. (C–H) Morphotype with delicate, fine-grained wall enclosing stercomata and sparse cytoplasm; all are from sample MC05. (I–K) Similar morphotype in which the wall includes an organic layer with finely agglutinated particles and gives rise to short filament-like structures; all are from sample MC05. Scale bars = 50 µm.

extensions with longitudinal striations and ending in a thin- Type B has relatively longer, narrower, and often somewhat walled bulb. This was by far the commonest form, particularly tapered tubular processes, sometimes ending in a small bulb. in the MC13 sample where it was represented by 174 specimens. Three specimens were found inside other structures in the MC11

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TABLE 5 | Absolute and relative abundance of complete foraminifera belonging to more robust (fossilizable) taxa, mainly multichambered.

>150 µm <150 µm Combined

‘Live’ Dead ‘Live’ Dead ‘Live’ Dead

N%N%N%N%N%N%

Rotaliids 19 22.1 24 15.1 41 18.6 24 5.80 60 19.6 48 8.38 Miliolids 0 0 3 1.89 6 2.73 0 0 6 1.96 3 0.52 Ammodiscids 0 0 9 5.66 2 0.91 25 6.04 2 0.65 34 5.93 Lageniids 0 0 1 0.63 6 2.73 8 1.93 6 1.96 9 1.57 Textulariids 4 4.65 36 22.6 9 4.09 87 21.0 13 4.24 123 21.5 Trochamminids 3 3.49 20 12.6 20 9.09 49 11.8 23 7.52 69 12.0 Hormosinids 29 33.7 48 30.2 42 19.1 96 23.2 71 23.2 144 25.1 Lagenammina 31 36.0 18 11.3 94 42.7 125 30.2 125 40.8 143 25.0 Total 86 159 220 414 306 573

The numbers are totals from all 5 samples. L = ‘Live’ (stained); D = Dead.

2 TABLE 6 | Number of morphospecies assigned to different foraminiferal corresponds to an overall density of 34.0 individuals per 10 cm . groups, and to gromiids. Nematodes were the most common metazoans (62.3%), followed by harpacticoid copepods (19.7%), nauplii (15.6%), 2 ostracods, 1 Foraminiferal group All species >150 µm <150 µm <150 only bivalve and 1 kinorhynch. Rotaliids 19 11 14 8 Miliolids 4 1 3 3 Ammodiscids 6 1 6 5 DISCUSSION Lageniids 5 3 5 2 Textulariids 32 13 24 18 Stained complete foraminiferal tests were more than an order Trochaminiids 18 10 16 8 of magnitude more abundant in our five sample splits from Hormosiniids 30 23 20 6 the eastern CCZ than metazoan meiofaunal animals (i.e., 2341 Lagenammina 15 4 13 11 stained tests compared with 167 metazoans, corresponding 2 Nodellum-like 17 8 15 8 to overall densities of 496 and 34 individuals per 10 cm , Flasks 4 3 4 1 respectively). The metazoan densities are generally lower than 2 Droplet chambers 2 0 2 2 those typical for the CCZ (11–394 individuals per 10 cm Chambers 2 tubes 2 0 2 0 in nine studies; summarized in Radziejewska, 2014, Table 3.4 Saccamminids 28 8 22 19 therein) and the mean values (88 ± 55 to 151 ± 54 individuals 2 Spheres 61 35 36 25 per 10 cm ) recently reported by Pape et al. (2017) from Organic-walled (allogromiids) 19 6 15 13 the GSR license area in the northeastern CCZ. Moreover, Hyperammina 6 3 3 3 the proportion (62.3%) of nematodes is relatively low and Tubes/spindles 77 54 57 20 the proportion of nauplii relatively high (15.6%), compared Other monothalamids 56 43 25 12 to previous studies. For example, nematodes represented 85– Chains 10 9 6 0 93% and nauplii 1.1–7.1% of the metazoan meiofauna in the Komoki-like 15 13 9 2 study of Pape et al. (2017). These discrepancies probably reflect Komoki: baculellids 19 19 9 0 methodological differences. In particular, while the 63 µm lower Komoki: komokiids 17 12 7 4 limit used in the present study is normal for foraminifera Total number of species 462 279 313 170 (Murray, 2014), it is not appropriate for analyzing metazoan Gromiids 8 0 8 8 meiofauna, for which 32 µm is now the generally accepted lower limit (Leduc et al., 2010). Nevertheless, although metazoans The numbers are totals from all 5 samples. were not adequately sampled, our results do suggest that stained foraminifera outnumber metazoan meiofaunal animals sample. Type C is spherical and was represented by 2 specimens in CCZ sediments. from the MC13 sample with several (3 and 5) rounded bumps on The nature of the organic-walled structures with blind-ending the surface of the organic wall. processes remains unresolved. They are almost certainly not A total of 167 metazoan meiofaunal organisms (not counting dinoflagellate cysts (Dr. Ian Harding, University of Southampton, 7 polychaete fragments without heads), all of which were well personal communication). The most likely identification, at least stained and assumed to have been alive when collected, were for the common forms from sample MC13 (Figures 5A–D), are picked from the 5 sample residues (i.e., 1/8th splits of the top 1- that they are metazoan eggs, possibly those of a crustacean (Dr. cm layer of five 10-cm diameter sediment cores). This number Manuel Bringué; Geological Survey of Canada – Calgary).

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TABLE 7 | Diversity metrics for the stained + dead assemblage in different samples.

MC09 MC11 MC05 MC13 MC21

UK-1 Stratum A UK-1 Stratum A UK-1 Stratum B UK-1 Stratum B OMS Stratum

>150 <150 Total >150 <150 Total >150 <150 Total >150 <150 Total >150 <150 Total

N 208 340 547 345 426 771 208 233 442 144 161 305 99 350 448 S 95 100 164 99 113 177 82 89 150 57 57 100 50 120 150

H’(loge) 4.27 4.03 4.59 3.96 4.07 4.55 3.95 4.02 4.52 3.57 3.22 3.96 3.53 4.19 4.38 Fisher α 67.6 47.7 85.0 47.2 50.2 74.0 49.9 52.6 83.1 37.3 32.1 56.9 40.3 64.5 79.1

E(S100) 63.6 52.0 63.3 50.4 52.2 60.2 52.4 54.9 62.1 46.7 44.0 53.0 50.0 56.0 59.0 R1D 7.21 9.71 6.63 10.14 12.7 7.03 6.44 12.4 6.58 24.1 44.7 26.1 15.1 10.0 7.81

TABLE 8 | Diversity metrics for the stained assemblage in different samples.

MC09 MC11 MC05 MC13 MC21

UK-1 Stratum A UK-1 Stratum A UK-1 Stratum B UK-1 Stratum B OMS Stratum

>150 <150 Total >150 <150 Total >150 <150 Total >150 <150 Total >150 <150 Total

N 152 171 323 292 307 597 123 167 290 85 114 199 42 170 212 S 74 72 129 80 87 144 61 61 115 30 36 57 26 70 83 0 H (loge) 4.03 3.844 4.438 3.69 3.756 4.260 3.69 3.635 4.293 2.883 2.492 3.209 3.072 3.820 3.851 Fisher α 58.7 46.29 84.92 36.3 40.93 60.27 36.35 35.19 69.52 16.20 18.77 27.40 29.11 44.25 51.89

E(S100) 58.8 52.3 65.1 44.2 47.6 54.2 44.2 47.0 59.8 30.0 34.2 39.60 26.0 51.7 52.75 R1D 7.89 11.6 10.9 12.0 17.3 8.88 8.12 16.5 9.18 24.1 46.8 27.1 9.52 11.7 17.1

The majority of complete stained (61.1%) as well as dead studies of abyssal Pacific samples. According to Snider et al. (63.8%) foraminiferal tests originated from the 63–150 µm (1984), spherical (‘sac-shaped’) morphotypes made up almost fractions. These results are consistent with previous studies third (31.3%) of meiofaunal foraminifera in the central North of deep-sea meiofauna, including foraminifera (e.g., Gooday, Pacific (5800 m depth). Nozawa et al. (2006), found an even 1986; Schewe, 2001), as well as with the general tendency for greater predominance (33.5 – 94.5%) of tiny, undescribed small-sized organisms to become increasingly important with ‘psammosphaerids’ in small samples from the Kaplan East increasing water depth (Thiel, 1975, 1983). Duchemin et al. site, located immediately to the west of the UK-1/OMS area (2007) report that the 63–150 µm fraction of the top 1-cm and at a similar water depth. The higher proportion probably of a core from 1000 m in the Bay of Biscay yielded the reflects the fact that Nozawa et al. (2006) examined even vast majority (97.5%) of stained foraminifera. In one of the finer fractions (>32 µm) fractions than those analyzed for most comprehensive studies, Phipps et al. (2012) found that the present study. Later, Ohkawara et al. (2009) established stained foraminiferal densities in the 63–150 µm fraction of a new species, Saccammina minimus, based on numerous samples taken along a down-slope transect (262 – 4987 m tiny agglutinated spheres from the deeper (∼5000 m) Kaplan water depth) on the Portuguese margin were consistently more Central site, located in the central part of the CCZ (∼14◦N, than twice those in the >150 µm fraction. Interestingly, the 130◦W). The majority of spheres in our samples are undescribed, proportion increased with depth, reaching a peak at 3908 m, but some are probably the same as S. minimus, while other where 88% of stained foraminifera were picked from the somewhat larger forms resemble Thurammina albicans. Small fine sieve residues. agglutinated spheres also occur in the abyssal North Atlantic. They represented 7.2 – 12.4% of assemblages >63 µm at the Porcupine and an even higher proportion (17.8%, Comparison With Modern Abyssal 21.0%) in two samples from the Cape Verde Abyssal Plain Assemblages (Gooday, 1996). Very small agglutinated tests were reported Fractions <150-µm were dominated by monothalamids, many of by Gooday et al. (1995) in North Atlantic sediments sieved them more or less spherical forms. These tiny spheres represented on 32 and 20 µm meshes. However, the spheres with a soft an average of 37.6 ± 8.1% of complete stained foraminifera in all ‘fluffy’ wall and containing stercomata (Figures 4C–K), which fractions combined and 49.4 ± 13.3% in the 63–150 µm fraction, are common in our samples, have not been observed in the with a significantly lower numbers in the 150–300 µm compared Atlantic material. to the 63–150 µm fraction (Table 1). Many have delicate, The finer residues yielded many tubular and spindle- fine-grained test walls and contain stercomata (Figures 4C–K). shaped morphotypes (Figure 3). Stained specimens judged Numerous agglutinated spheres are also reported in previous to be complete were again more common in the >150-µm

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FIGURE 5 | Unidentified organic-walled structures (?metazoan eggs) from 63–125 µm fractions. (A–C) Type A with short striated tubes ending in thin-walled bulbs; MC11, 0–0.5 cm layer. (D,E) Type B with relatively long slender tubes, sometimes ending in a small thin-walled bulb; MC11, 0–0.5 cm. (F) Type C with rounded bumps; MC13, 0.5–1.0 cm layer. Scale bars = 50 µm.

(mean 21.4%) than the <150-µm (mean 6.12%) fraction samples (42–1000-µm fraction). Based on the conservative (Table 3). Tubular fragments (stained as well as stained and assumption that all fragments of a similar type within a sediment dead combined) were also very numerous, representing >60% layer and adjacent layers were derived from one individual, they in both size fractions (Supplementary Table S2). Similar calculated that 24% of monothalamids were tubular forms. fragments are often common in abyssal samples. Bernstein Our samples also yielded small, multichambered foraminfera et al. (1978) recorded 30,938 fragments compared to 5,079 that are similar to those reported in previous studies of modern complete foraminiferal tests in 5 unstained box-corer residues abyssal benthic foraminifera. They include agglutinated species (>297 µm fraction) from the central North Pacific. Snider et al. (e.g., Cribrostomoides subglobosum, trullisata, (1984) likewise found numerous fragments in their North Pacific Cystammina galatea, Cystammina pauciloculata, Deuterammina

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grahami, Glomospira spp., Hormosinella ovicula, Hyperammina of which reveal different species-level responses to food inputs cylindrica, Lagenammina difflugiformis, Paratrochammina (Nomaki et al., 2005, 2006). scotiaensis, Reophax scorpiurus, Spiroplectammina subcylindrica, The deposition of phytodetritus on the deep-sea floor is Hormosinella distans, Veleroninoides wiesneri), and calcareous well documented at temperate latitudes in the NE Atlantic. species [Epistominella exigua, Nuttallides umbonatus, In the Pacific the phenomenon is reported from various sites Cibicidoides mundulus (as C. cf mundulus), Fissurina staphyllearia along the North American continental margin (Beaulieu, 2002), and Melonis pompiliodes] previously reported from abyssal notably at the intensively studied abyssal (4100 m depth) Station depths in the North and equatorial Pacific by authors such as M on the Californian margin (Beaulieu and Smith, 1998). Smith (1973), Burministrova et al. (2007), and Enge et al. (2012). Here, as in the NE Atlantic, the presence of these deposits Many of these are well-known morphospecies that are widely on the seafloor has a distinct seasonal component (Lauerman distributed in modern ocean basins (Gooday and Jorissen, 2012; and Kaufmann, 1998). There is also evidence for seafloor Holbourn et al., 2013). phytodetritus in the abyssal equatorial Pacific. Deposition in this open ocean setting, however, is not seasonal (Beaulieu, 2002) and Comparison With Fossil Assemblages is linked to upwelling created by easterly trade winds (Smith and Demopoulos, 2003). Gardner et al. (1984) observed ‘dark There are some similarities between the agglutinated foraminifera globs of material’ that were ‘1–4 cm across and appear fluffy in our samples and certain assemblages of multichambered taxa and organic in nature...’ in seafloor photographs taken at a of Late and Paleogene age recovered in Deep-Sea site to the south of the central CCZ (4◦N, 136◦W; 4469 m Drilling Project (DSDP) and Ocean Drilling Project (ODP) depth). Smith et al. (1996) recovered phytodetritus in multicore cores. Krasheninnikov described Upper Cretaceous faunas samples collected along the 140◦W line from 5◦N to 5◦S. Further devoid of calcareous foraminifera in red-brown clays from east, and within the CCZ, Radziejewska (2002) observed a the Pacific (1973) and Indian (1974) Oceans. He interpreted ‘very thin layer of a fluffy material, greenish-brown in color’ these as having been deposited in oceanic sediments below (i.e., phytodetritus) on the surfaces of some cores collected in the CCD. They consisted mainly of small species, often with 1997 in part of the IOM contract area (centered at 11◦ 040N, smooth, fine-grained test walls, assigned to genera such as 119◦ 400W; 4380–4430 m depth) that had been subject 2 years Haplophragmoides, Labrospira, Trochammina, and Recurvoides. earlier to an experimental disturbance designed to simulate Similar abyssal faunas are known from the North Atlantic the effects of nodule mining (see also Radziejewska, 2014). Plantagenet Formation, where they also include ‘rhizamminids’ Samples of this material, which was very patchily distributed, and ‘fossil forms which resemble modern Komokiaceans’ (Kuhnt contained chloropigments and intact . Phytodetritus et al., 1989). However, our multichambered assemblages also was not present on the surfaces of cores recovered in 1995 contain some calcareous taxa (mainly rotaliids), reflecting or 2000. Its presence in 1997 was believed to be largely their location close to, rather than well below, the CCD. responsible for the greatly increased abundance of the nematode In this respect, they have more in common with the genera Desmoscolex and Pareudesmoscolex compared to 1995 mixed calcareous and agglutinated assemblages described by (Radziejewska et al., 2001). Increases in metazoan megafauna in Hemleben and Troester (1984) from DSDP Hole 543A in the nodule-bearing parts of the IOM area was likewise attributed to central Atlantic. the increased food supply originating from phytodetrital inputs Species of Reophax and other hormosinids, which consistently (Radziejewska and Stoyanova, 2000). constitute the most common multichambered foraminifera in Small lumps of phytodetritus-like material were occasionally our samples, are often not well represented in the Late Cretaceous found in our sieve residues, but these deposits were not assemblages, possibly a result of the low fossilization potential observed on the surfaces of any megacores collected during the of their fairly delicate tests (Schröder, 1986). Some more robust present study. However, our residues yielded small numbers species, however, are preserved as fossils in deep-sea sediments of species, notably Alabaminella weddellensis and Epistominella (e.g., Kuhnt and Moullade, 1991). exigua, which are known to exploit phytodetritual inputs in the abyssal NE Atlantic (e.g., Gooday, 1988, 1993). Epistominella Possible Ecological Significance exigua, in particular, contained bright green cytoplasm indicating Responses to Food Inputs ingestion of fresh chlorophyll-bearing particles (Figure 2A). One rationale for including finer sieve fractions (63–150 µm) in Darker green cytoplasm is typical of Nuttallides umbonifera, ecological studies of bathyal and abyssal foraminifera is that small the most common rotaliid in our samples (Supplementary species often display opportunistic responses to seasonally pulsed Figure S3D). If inputs of phytodetritus do occur from time food (‘phytodetritus’) inputs to the seafloor (e.g., Gooday, 1988, to time in the UK and OMS claim areas, as they appear to 2003; Gooday and Lambshead, 1989; Corliss and Silva, 1993; Silva do in the nearby IOM area, then these and perhaps other et al., 1996; Ohga and Kitazato, 1997; Gooday and Rathburn, species are likely to respond to this fresh food source with 1999; Gooday and Hughes, 2002; Kitazato et al., 2003; Heinz and rapid reproduction and population growth. All but 2 of the 25 Hemleben, 2006; Duchemin et al., 2007). This suggests that they specimens (stained and dead) of A. weddellensis and E. exigua play an active role in the processing fresh organic carbon on were extracted from residues <150 µm, demonstrating the the ocean floor, an inference supported by in situ experimental importance of examining finer sediment fractions in order to studies using 13C-labeled algae (Moodley et al., 2002), some recover small, opportunistic foraminiferal species that may be

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important players in the processing of fresh organic matter on CONCLUSION the ocean floor. Is the considerable additional effort required to analyze Possible Importance in Recolonization foraminifera in 63–150 µm fractions of samples from areas Alve (1999) reviewed how sediments that have been defaunated that could be disturbed by seabed mining worthwhile? In the by natural or anthropogenic processes can be repopulated present study, the fine-fraction assemblages contained >60% by benthic foraminifera. In relatively tranquil settings, initial of stained and dead test as well as 170 species that were recolonization may proceed in a series of stages, starting with not present in the coarser fractions. They also yielded quick-growing, opportunists that are succeeded by slower- greater absolute abundances than >150-µm fractions of several growing, more specialized species. Relatively few studies of monothalamid groups, notably Lagenammina spp., Nodellum- foraminiferal recolonization have been conducted in deep- like forms, saccamminids, and particularly spherical forms, as water settings. Probably the best direct evidence comes from well as some multichambered taxa, namely rotaliids (stained samples collected during 5 cruises (spring 1994, summer and only), hormosinids (dead only), textulariids (dead only), winter 1996, summer 1998, spring 1999) in an area of the and trochamminids. An important part of the foraminiferal South China Sea (∼2500 m depth) blanketed by a layer assemblage was therefore confined to these fine fractions. of volcanic ash from the 1991 Mt Pinatubo eruption (Hess As argued elsewhere (e.g., Gooday et al., 2008; Goineau and Kuhnt, 1996; Hess et al., 2001; Kuhnt et al., 2005). and Gooday, 2017), multichambered taxa, particularly the Although the material involved was different, the ash fall to calcareous rotaliids, may be metabolically more active than some extent mimicked the deposition of resuspended sediment stercomata-bearing monothalamids in deep-sea settings, and expected to result from seabed mining. In samples sieved on therefore more important in terms of ecosystem functioning. a 63-µm mesh, the initial recolonizers of the 2- to 6-cm- Although rotaliids are relatively uncommon in our samples, their thick ash layer appeared to be a small species of Textularia, greater absolute (but not relative) abundance in the <150-µm followed by Reophax dentaliniformis and later by R. bilocularis fractions provides one incentive for analyzing fine sieve residues. and R. scorpiurus, the rotaliid Bolivina difformis and the Another justification is the potentially important role that miliolid Quinqueloculina seminula (Hess et al., 2001). A second small multichambered opportunistic species could play in the wave of recolonizers included Trochammina spp., Adercotryma recolonization of sediments disturbed by mining. Nevertheless, glomerata, and Subreophax guttifera. the fact remains that this work is very time-consuming and Analysis of sediments deposited by turbidity currents in difficult to undertake routinely. submarine canyons has provided insights into the recolonization A number of studies have used foraminiferal faunal data and by foraminifera of physically disturbed areas of seafloor. diversity metrics as bio-indicators of human impacts in marine According to Duros et al. (2017), the initial recolonizers in environments (e.g., Jorissen et al., 2009 and references therein). the >150 µm fraction of a turbidite deposit at upper bathyal This has led to the formulation of a series of recommendations, depths (983 m, 1454 m) in the Capbreton Canyon (Bay of Biscay) the FOMIBO initiative, aimed at standardizing methodologies were Fursenkoina bradyi, R. dentaliniformis and Technitella melo. applied in such studies (Schönfeld et al., 2012). One of the However, the 63–150 µm fraction from the 983-m site, as well as ‘mandatory’ recommendations is that, although samples should two shallower sites (251 m, 301 m), were dominated by juveniles be sieved on a 63-µm mesh, detailed analysis should be based of Bolivina subaenariensis, which was interpreted as representing on the >125-µm fraction. However, they also add the ‘advisory’ a second stage of recolonization. The same species dominated recommendation that in some eutrophic settings, where small low diversity assemblages (63–150-µm fraction) of two cores opportunistic species are abundant, it may also be necessary collected in the same canyon at a 600 m site that had been to analyze the finer 63–125-µm as well as the >125 µm impacted by a turbidity current 1.5 years earlier (Hess et al., 2005; fraction. A similar conclusion was reached by Sen Gupta et al. Hess and Jorissen, 2009). Here, B. subaenariensis may have been (1987). A sensible compromise in the case of baseline studies responding to organic matter associated with the turbidite, as well of foraminifera in Pacific nodule fields would therefore be as participating in the recolonization process. to concentrate efforts on analyzing coarser residues from all These studies suggest that azoic substrates, originating either samples but to examine finer fractions (63–150 µm), either from deposited material (ash) or physical disturbance of the quantitatively or qualitatively, in a subset of samples or sample seafloor (turbidite), are colonized by a succession of foraminiferal splits. Similar approaches have been adopted by a number of species. In both cases, the colonizing species were considered authors working in the NE Atlantic deep-sea samples (e.g., Phipps to have been infaunal. Some of these species are larger (e.g., et al., 2012; Duros et al., 2017). It may be particularly important Reophax spp., which are fairly common in our samples) and to do this during monitoring exercises, i.e., where deep-sea more likely to be retained in the >150-µm fraction, but sediments have been defaunated by seabed mining and are in smaller species or juveniles are also involved. Our finer fractions the early stages of recolonization by meiofaunal organisms. To yielded small agglutinated species belonging to genera such as conclude, foraminifera and particularly monothalamids are a Ammobaculites, Spiroplectammina, and Textularia that are rare major constituent of benthic faunas in the CCZ nodule fields. in the stained assemblages. It is possible that such species may Despite the methodological challenges that they pose, we would be important during initial phases of recolonization following encourage other researchers to consider including them in studies mining-related disturbances. of areas where seabed mining may occur in the future.

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DATA AVAILABILITY ACKNOWLEDGMENTS

All datasets generated for this study are included in the We are grateful to Craig Smith for his leadership of manuscript and/or the Supplementary Files. the overall ABYSSLINE project and particularly the AB01 and AB02 cruises, as well as Ivan Voltski (AB01) and Alexandra Weber (AB02) for their help with core collection AUTHOR CONTRIBUTIONS and processing at sea. We would like to thank Dr. Ian Harding and Dr. Manuel Bringué for their advice regarding AJG conceived the project, analyzed the <150 µm fractions, the identity of the unidentified organic-walled structures and prepared the figures and tables. AG analyzed the >150 µm and two reviewers for their comments, which helped to fractions. Both authors integrated and analyzed the <150 µm and improve the manuscript. >150 µm fraction data. The manuscript was largely written by AG with contributions from AJG. SUPPLEMENTARY MATERIAL FUNDING The Supplementary Material for this article can be found The ABYSSLINE project was funded through a commercial online at: https://www.frontiersin.org/articles/10.3389/fmars. arrangement with UK Seabed Resources Ltd. 2019.00114/full#supplementary-material

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